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Stem Cells International
Volume 2014, Article ID 653734, 9 pages
http://dx.doi.org/10.1155/2014/653734
Research Article

Evidence for Transfer of Membranes from Mesenchymal Stem Cells to HL-1 Cardiac Cells

1Department of Biology, Trinity Christian College, Palos Heights, IL 60463, USA
2Physician Assistant Studies/Allied Health Sciences, College of Health Professions, Grand Valley State University, Grand Rapids, IL 49503, USA

Received 30 June 2014; Revised 13 August 2014; Accepted 18 August 2014; Published 9 September 2014

Academic Editor: Gary E. Lyons

Copyright © 2014 Robert A. Boomsma and David L. Geenen. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. A. Boomsma, P. D. Swaminathan, and D. L. Geenen, “Intravenously injected mesenchymal stem cells home to viable myocardium after coronary occlusion and preserve systolic function without altering infarct size,” International Journal of Cardiology, vol. 122, no. 1, pp. 17–28, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. R. A. Boomsma and D. L. Geenen, “Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis,” PloS one, vol. 7, no. 4, Article ID e35685, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. J. S. Burchfield and S. Dimmeler, “Role of paracrine factors in stem and progenitor cell mediated cardiac repair and tissue fibrosis,” Fibrogenesis Tissue Repair, vol. 1, no. 1, p. 4, 2008. View at Google Scholar
  4. J. E. Saffitz, K. Y. Hames, and S. Kanno, “Remodeling of gap junctions in ischemic and nonischemic forms of heart disease,” Journal of Membrane Biology, vol. 218, no. 1–3, pp. 65–71, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Kar, N. Batra, M. A. Riquelme, and J. X. Jiang, “Biological role of connexin intercellular channels and hemichannels,” Archives of Biochemistry and Biophysics, vol. 524, no. 1, pp. 2–15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Abbaci, M. Barberi-Heyob, W. Blondel, F. Guillemin, and J. Didelon, “Advantages and limitations of commonly used methods to assay the molecular permeability of gap junctional intercellular communication,” BioTechniques, vol. 45, no. 1, pp. 33–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Valiunas, S. Doronin, L. Valiuniene et al., “Human mesenchymal stem cells make cardiac connexins and form functional gap junctions,” The Journal of Physiology, vol. 555, part 3, pp. 617–626, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Mureli, C. P. Gans, D. J. Bare, D. L. Geenen, N. M. Kumar, and K. Banach, “Mesenchymal stem cells improve cardiac conduction by upregulation of connexin 43 through paracrine signaling,” The American Journal of Physiology: Heart and Circulatory Physiology, vol. 304, no. 4, pp. H600–H609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. J.-Y. Hahn, H.-J. Cho, H.-J. Kang et al., “Pre-treatment of mesenchymal stem cells with a combination of growth factors enhances gap junction formation, cytoprotective effect on cardiomyocytes, and therapeutic efficacy for myocardial infarction,” Journal of the American College of Cardiology, vol. 51, no. 9, pp. 933–943, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Abounit and C. Zurzolo, “Wiring through tunneling nanotubes—from electrical signals to organelle transfer,” Journal of Cell Science, vol. 125, part 5, pp. 1089–1098, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Katsuda, N. Kosaka, F. Takeshita, and T. Ochiya, “The therapeutic potential of mesenchymal stem cell-derived extracellular vesicles,” Proteomics, vol. 13, no. 10-11, pp. 1637–1653, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. H.-H. Gerdes, A. Rustom, and X. Wang, “Tunneling nanotubes, an emerging intercellular communication route in development,” Mechanisms of Development, vol. 130, no. 6–8, pp. 381–387, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. S. F. Mause and C. Weber, “Microparticles: protagonists of a novel communication network for intercellular information exchange,” Circulation Research, vol. 107, no. 9, pp. 1047–1057, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Mittelbrunn and F. Sánchez-Madrid, “Intercellular communication: diverse structures for exchange of genetic information,” Nature Reviews Molecular Cell Biology, vol. 13, no. 5, pp. 328–335, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. X. Liang, Y. Ding, Y. Zhang, H. F. Tse, and Q. Lian, “Paracrine mechanisms of Mesenchymal Stem cell-based therapy: current status and perspectives,” Cell Transplant, 2013. View at Publisher · View at Google Scholar
  16. F. Arslan, R. C. Lai, M. B. Smeets et al., “Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury,” Stem Cell Research, vol. 10, no. 3, pp. 301–312, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Y. Plotnikov, T. G. Khryapenkova, A. K. Vasileva et al., “Cell-to-cell cross-talk between mesenchymal stem cells and cardiomyocytes in co-culture,” Journal of Cellular and Molecular Medicine, vol. 12, no. 5, pp. 1622–1631, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Acquistapace, T. Bru, P.-F. Lesault et al., “Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer,” Stem Cells, vol. 29, no. 5, pp. 812–824, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Figeac, P. F. Lesault, O. Le Coz et al., “Nanotubular crosstalk with distressed cardiomyocytes stimulates the paracrine repair function of mesenchymal stem cells,” Stem Cells, vol. 32, no. 1, pp. 216–230, 2014. View at Publisher · View at Google Scholar
  20. W. C. Claycomb, N. A. Lanson Jr., B. S. Stallworth et al., “HL-1 cells: A cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 6, pp. 2979–2984, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. D. L. Boger, J. E. Patterson, X. Guan, B. F. Cravatt, R. A. Lerner, and N. B. Gilula, “Chemical requirements for inhibition of gap junction communication by the biologically active lipid oleamide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 9, pp. 4810–4815, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. G. R. Juszczak and A. H. Swiergiel, “Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: animal and human studies,” Progress in Neuro-Psychopharmacology & Biological Psychiatry, vol. 33, no. 2, pp. 181–198, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Zou, X. Y. Yue, S. C. Zheng et al., “Cholesterol modulates function of connexin 43 gap junction channel via PKC pathway in H9c2 cells,” Biochimica et Biophysica Acta, vol. 1838, no. 8, pp. 2019–2025, 2014. View at Google Scholar
  24. Z. Ma, H. Yang, H. Liu et al., “Mesenchymal stem cell-cardiomyocyte interactions under defined contact modes on laser-patterned biochips,” PLoS ONE, vol. 8, no. 2, Article ID e56554, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Strassburg, N. W. Hodson, P. I. Hill, S. M. Richardson, and J. A. Hoyland, “Bi-directional exchange of membrane components occurs during co-culture of mesenchymal stem cells and nucleus pulposus cells,” PLoS ONE, vol. 7, no. 3, Article ID e33739, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Dimmeler, A. M. Zeiher, and M. D. Schneider, “Unchain my heart: the scientific foundations of cardiac repair,” Journal of Clinical Investigation, vol. 115, no. 3, pp. 572–583, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Alvarez-Dolado, R. Pardal, J. M. Garcia-Verdugo et al., “Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes,” Nature, vol. 425, no. 6961, pp. 968–973, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Tsuji, S. Miyoshi, Y. Ikegami et al., “Xenografted human amniotic membrane-derived mesenchymal stem cells are immunologically tolerated and transdifferentiated into cardiomyocytes,” Circulation Research, vol. 106, no. 10, pp. 1613–1623, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. D. J. Maltman, S. A. Hardy, and S. A. Przyborski, “Role of mesenchymal stem cells in neurogenesis and nervous system repair,” Neurochemistry International, vol. 59, no. 3, pp. 347–356, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Grajales, J. García, K. Banach, and D. L. Geenen, “Delayed enrichment of mesenchymal cells promotes cardiac lineage and calcium transient development,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 4, pp. 735–745, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Grajales, J. García, and D. L. Geenen, “Induction of cardiac myogenic lineage development differs between mesenchymal and satellite cells and is accelerated by bone morphogenetic protein-4,” Journal of Molecular and Cellular Cardiology, vol. 53, no. 3, pp. 382–391, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. Y.-H. Choi, A. Kurtz, and C. Stamm, “Mesenchymal stem cells for cardiac cell therapy,” Human Gene Therapy, vol. 22, no. 1, pp. 3–17, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Gnecchi, Z. Zhang, A. Ni, and V. J. Dzau, “Paracrine mechanisms in adult stem cell signaling and therapy,” Circulation Research, vol. 103, no. 11, pp. 1204–1219, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. A. A. Ramkisoensing, D. A. Pijnappels, J. Swildens et al., “Gap junctional coupling with cardiomyocytes is necessary but not sufficient for cardiomyogenic differentiation of cocultured human mesenchymal stem cells,” Stem Cells, vol. 30, no. 6, pp. 1236–1245, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Waldenström, N. Gennebäck, U. Hellman, and G. Ronquist, “Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells,” PLoS ONE, vol. 7, no. 4, Article ID e34653, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. X. Wang and H.-H. Gerdes, “Long-distance electrical coupling via tunneling nanotubes,” Biochimica et Biophysica Acta: Biomembranes, vol. 1818, no. 8, pp. 2082–2086, 2012. View at Publisher · View at Google Scholar · View at Scopus